Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis

Summary: Transposable elements (TEs) are abundant in metazoan genomes and have multifaceted effects on host fitness. However, the mechanisms underlying the functions of TEs are still not fully understood. Here, we combine Hi-C, ATAC-seq, and ChIP-seq assays to report the existence of multimegabase s...

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Main Authors: Zhaoying Shi, Jinsheng Xu, Longjian Niu, Wei Shen, Shuting Yan, Yongjun Tan, Xuebo Quan, Edwin Cheung, Kai Huang, Yonglong Chen, Li Li, Chunhui Hou
Format: Article
Language:English
Published: Elsevier 2023-03-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124723001626
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author Zhaoying Shi
Jinsheng Xu
Longjian Niu
Wei Shen
Shuting Yan
Yongjun Tan
Xuebo Quan
Edwin Cheung
Kai Huang
Yonglong Chen
Li Li
Chunhui Hou
author_facet Zhaoying Shi
Jinsheng Xu
Longjian Niu
Wei Shen
Shuting Yan
Yongjun Tan
Xuebo Quan
Edwin Cheung
Kai Huang
Yonglong Chen
Li Li
Chunhui Hou
author_sort Zhaoying Shi
collection DOAJ
description Summary: Transposable elements (TEs) are abundant in metazoan genomes and have multifaceted effects on host fitness. However, the mechanisms underlying the functions of TEs are still not fully understood. Here, we combine Hi-C, ATAC-seq, and ChIP-seq assays to report the existence of multimegabase supersized loop (SSL) clusters in the Xenopus tropicalis sperm. We show that SSL anchors are inaccessible and devoid of the architectural protein CTCF, RNA polymerase II, and modified histones. Nearly all SSL anchors are marked by Helitrons, a class II DNA transposon. Molecular dynamics simulations indicate that SSL clusters are likely formed via a molecular agent-mediated chromatin condensation process. However, only slightly more SSL anchor-associated genes are expressed at late embryo development stages, suggesting that SSL anchors might only function in sperm. Our work shows an evolutionarily distinct and sperm-specific genome structure marked by a subset of Helitrons, whose establishment and function remain to be explored.
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spelling doaj.art-c5ea80c57a604a68966ea98014a386d62023-02-24T04:30:40ZengElsevierCell Reports2211-12472023-03-01423112151Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalisZhaoying Shi0Jinsheng Xu1Longjian Niu2Wei Shen3Shuting Yan4Yongjun Tan5Xuebo Quan6Edwin Cheung7Kai Huang8Yonglong Chen9Li Li10Chunhui Hou11Department of Biology, Southern University of Science and Technology, Shenzhen 518055, ChinaDepartment of Bioinformatics, Huazhong Agricultural University, Wuhan 430070, China; Hubei Key Laboratory of Agricultural Bioinformatics, Huazhong Agricultural University, Wuhan 430070, ChinaChina State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; School of Public Health and Emergency Management, Southern University of Science and Technology, Shenzhen 518055, China; Shenzhen Key Laboratory of Cardiovascular Health and Precision Medicine, Southern University of Science and Technology, Shenzhen 518055, ChinaDepartment of Bioinformatics, Huazhong Agricultural University, Wuhan 430070, China; Hubei Key Laboratory of Agricultural Bioinformatics, Huazhong Agricultural University, Wuhan 430070, ChinaInstitute of Systems and Physical Biology, Shenzhen Bay Laboratory, Shenzhen 518132, ChinaDepartment of Biology, Southern University of Science and Technology, Shenzhen 518055, China; China State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, ChinaInstitute of Systems and Physical Biology, Shenzhen Bay Laboratory, Shenzhen 518132, ChinaCancer Centre, Faculty of Health Sciences, University of Macau, Taipa, Macau 999078, China; Frontier Science Centre for Precision Oncology of Ministry of Education, University of Macau, Taipa, Macau 999078, ChinaInstitute of Systems and Physical Biology, Shenzhen Bay Laboratory, Shenzhen 518132, China; Corresponding authorDepartment of Biology, Southern University of Science and Technology, Shenzhen 518055, China; Corresponding authorDepartment of Bioinformatics, Huazhong Agricultural University, Wuhan 430070, China; Hubei Key Laboratory of Agricultural Bioinformatics, Huazhong Agricultural University, Wuhan 430070, China; Corresponding authorChina State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Corresponding authorSummary: Transposable elements (TEs) are abundant in metazoan genomes and have multifaceted effects on host fitness. However, the mechanisms underlying the functions of TEs are still not fully understood. Here, we combine Hi-C, ATAC-seq, and ChIP-seq assays to report the existence of multimegabase supersized loop (SSL) clusters in the Xenopus tropicalis sperm. We show that SSL anchors are inaccessible and devoid of the architectural protein CTCF, RNA polymerase II, and modified histones. Nearly all SSL anchors are marked by Helitrons, a class II DNA transposon. Molecular dynamics simulations indicate that SSL clusters are likely formed via a molecular agent-mediated chromatin condensation process. However, only slightly more SSL anchor-associated genes are expressed at late embryo development stages, suggesting that SSL anchors might only function in sperm. Our work shows an evolutionarily distinct and sperm-specific genome structure marked by a subset of Helitrons, whose establishment and function remain to be explored.http://www.sciencedirect.com/science/article/pii/S2211124723001626CP: Molecular biology
spellingShingle Zhaoying Shi
Jinsheng Xu
Longjian Niu
Wei Shen
Shuting Yan
Yongjun Tan
Xuebo Quan
Edwin Cheung
Kai Huang
Yonglong Chen
Li Li
Chunhui Hou
Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis
Cell Reports
CP: Molecular biology
title Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis
title_full Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis
title_fullStr Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis
title_full_unstemmed Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis
title_short Evolutionarily distinct and sperm-specific supersized chromatin loops are marked by Helitron transposons in Xenopus tropicalis
title_sort evolutionarily distinct and sperm specific supersized chromatin loops are marked by helitron transposons in xenopus tropicalis
topic CP: Molecular biology
url http://www.sciencedirect.com/science/article/pii/S2211124723001626
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